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Untargeted Alternative Routes of Arbovirus Transmission

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A special issue of Pathogens (ISSN 2076-0817).

Deadline for manuscript submissions: closed (31 July 2020) | Viewed by 49767

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Special Issue Editor

Dr. Julien Pompon

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Guest Editor

MIVEGEC, IRD, Montpellier, France
Interests: Aedes; arboviruses; transmission; molecular mechanisms of transmission

Special Issue Information

Dear Colleagues,

Arboviruses have emerged as global pathogens of significant importance in the past 50 years. Globalization, unplanned urbanization, and climate change have all contributed to their development. The main culprits are mosquitoes, mostly from the species Aedes aegypti, which transmit these viruses. These mosquitoes thrive in man-made environments and have been dispersed throughout the world by global transport. Their ecological acquaintance with and proclivity to bite humans, together with their susceptibility to arbovirus replication, make them an ideal vector. Consequently, Ae. aegypti is considered to be the primary vector for flaviviruses, such as dengue, Zika, and yellow fever, and alphaviruses, such as chikungunya virus and Mayaro virus. All of these viruses cause flu-like symptoms that can develop into life-threatening (hemorrhaging for flaviviruses) or life-debilitating (arthralgia for alphaviruses) conditions. Because of the worldwide distribution of Ae. aegypti, close to half of the world population is at risk of being infected. Dengue virus (DENV) is the most widespread arbovirus and infects an estimated 400 million people per year, while Zika virus (ZIKV) became famous after its rapid spreading in South America, where close to 70% of the population was infected in just 4 years.

This alarming situation has stimulated research to develop control methods. The difficulty of developing an effective vaccine (see the last DENV vaccine developed by Sanofi-Pasteur) and therapeutic treatments favors interventions targeting the vector using transgenic, radiation, or microbiome modifications of Ae. aegypti populations. The most promising tools make use of the bacterium Wolbachia to sterilize progeny to suppress populations or to reduce virus replication to block transmission. Both strategies are being tested in field trials and have shown that they can be deployed to restrict transmission at least in a restricted area. However, these vector-based interventions mainly target the main vector, Ae. aegypti, making room for so-called “secondary” or alternative routes of transmission to become preponderant.

With regards to the potential for these new tools to significantly reduce the global burden of arboviruses, we believe that it is time to gather information about the “Untargeted Alternative Routes of Arbovirus Transmission”, because these alternative routes may become significant to arbovirus epidemiology. In this context, Pathogens is launching a Special Issue on this topic, and submissions, including research articles, short communications, and reviews describing the state of the art and recent developments with respect to these alternative routes, are welcome. At this time, when promising tools are under field development, knowledge about potential substitutive transmission routes will help devise long-term control measures to sustain low arbovirus transmission.

Both original research and review articles are welcome. Potential topics include, but are not limited to, the following:

Newly emerging viruses;
Secondary/alternative vectors;
Non-horizontal transmission;
Undocumented epidemics.

Dr. Julien Pompon
Guest Editor

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Keywords

arbovirus
mosquito
Aedes
vector competence
vector capacity

Published Papers (10 papers)

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Research

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13 pages, 1325 KiB

Open AccessArticle

Vector Competence for Dengue-2 Viruses Isolated from Patients with Different Disease Severity

by Ronald Enrique Morales-Vargas, Dorothée Missé, Irwin F. Chavez and Pattamaporn Kittayapong

Pathogens 2020, 9(10), 859; https://doi.org/10.3390/pathogens9100859 - 21 Oct 2020

Cited by 4 | Viewed by 2331

Abstract

Dynamics of dengue serotype 2 virus isolated from patients with different disease severity, namely flu-like classic dengue fever (DF) and dengue shock syndrome (DSS) were studied in its mosquito vector Aedes aegypti. We compared isolate infectivity and vector competence (VC) among thirty two A. aegypti-viral isolate pairs. Mosquito populations from high dengue incidence area exhibited overall greater VC than those from low dengue incidence area at 58.1% and 52.5%, respectively. On the other hand, the overall infection rates for the isolates ThNR2/772 (DF, 62.3%) and ThNR2/391 (DSS, 60.9%), were significantly higher than those for isolates ThNR2/406 (DF, 55.2%) and ThNR2/479 (DSS, 54.8%). These results suggest that the efficacy of dengue virus circulation was likely to vary according to the combination between the virus strains and origin of the mosquito strains, and this may have epidemiologic implications toward the incidence of flu-like classic dengue fever (DF) and dengue shock syndrome (DSS). Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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18 pages, 2649 KiB

Open AccessEditor’s ChoiceArticle

Trends of the Dengue Serotype-4 Circulation with Epidemiological, Phylogenetic, and Entomological Insights in Lao PDR between 2015 and 2019

by Elodie Calvez, Virginie Pommelet, Somphavanh Somlor, Julien Pompon, Souksakhone Viengphouthong, Phaithong Bounmany, Thep Aksone Chindavong, Thonglakhone Xaybounsou, Phoyphaylinh Prasayasith, Sitsana Keosenhom, Paul T. Brey, Olivier Telle, Marc Choisy, Sébastien Marcombe and Marc Grandadam

Pathogens 2020, 9(9), 728; https://doi.org/10.3390/pathogens9090728 - 3 Sep 2020

Cited by 12 | Viewed by 4718

Abstract

Dengue outbreaks have regularly been recorded in Lao People’s Democratic Republic (PDR) since the first detection of the disease in 1979. In 2012, an integrated arbovirus surveillance network was set up in Lao PDR and an entomological surveillance has been implemented since 2016 in Vientiane Capital. Here, we report a study combining epidemiological, phylogenetic, and entomological analyzes during the largest DENV-4 epidemic ever recorded in Lao PDR (2015–2019). Strikingly, from 2015 to 2019, we reported the DENV-4 emergence and spread at the country level after two large epidemics predominated by DENV-3 and DENV-1, respectively, in 2012–2013 and 2015. Our data revealed a significant difference in the median age of the patient infected by DENV-4 compared to the other serotypes. Phylogenetic analysis demonstrated the circulation of DENV-4 Genotype I at the country level since at least 2013. The entomological surveillance showed a predominance of Aedesaegypti compared to Aedesalbopictus and high abundance of these vectors in dry and rainy seasons between 2016 and 2019, in Vientiane Capital. Overall, these results emphasized the importance of an integrated approach to evaluate factors, which could impact the circulation and the epidemiological profile of dengue viruses, especially in endemic countries like Lao PDR. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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17 pages, 1934 KiB

Open AccessEditor’s ChoiceArticle

Vector Competence of Aedes aegypti, Aedes albopictus and Culex quinquefasciatus from Brazil and New Caledonia for Three Zika Virus Lineages

by Rosilainy S. Fernandes, Olivia O’Connor, Maria Ignez L. Bersot, Dominique Girault, Marguerite R. Dokunengo, Nicolas Pocquet, Myrielle Dupont-Rouzeyrol and Ricardo Lourenço-de-Oliveira

Pathogens 2020, 9(7), 575; https://doi.org/10.3390/pathogens9070575 - 16 Jul 2020

Cited by 17 | Viewed by 3255

Abstract

Zika virus (ZIKV) has caused severe epidemics in South America beginning in 2015, following its spread through the Pacific. We comparatively assessed the vector competence of ten populations of Aedes aegypti and Ae. albopictus from Brazil and two of Ae. aegypti and one of Culex quinquefasciatus from New Caledonia to transmit three ZIKV isolates belonging to African, Asian and American lineages. Recently colonized mosquitoes from eight distinct sites from both countries were orally challenged with the same viral load (10⁷ TCID₅₀/mL) and examined after 7, 14 and 21 days. Cx. quinquefasciatus was refractory to infection with all virus strains. In contrast, although competence varied with geographical origin, Brazilian and New Caledonian Ae. aegypti could transmit the three ZIKV lineages, with a strong advantage for the African lineage (the only one reaching saliva one-week after challenge). Brazilian Ae. albopictus populations were less competent than Ae. aegypti populations. Ae. albopictus generally exhibited almost no transmission for Asian and American lineages, but was efficient in transmitting the African ZIKV. Viral surveillance and mosquito control measures must be strengthened to avoid the spread of new ZIKV lineages and minimize the transmission of viruses currently circulating. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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11 pages, 2270 KiB

Open AccessArticle

Entomological Surveillance for Zika and Dengue Virus in Aedes Mosquitoes: Implications for Vector Control in Thailand

by Nathamon Kosoltanapiwat, Jarinee Tongshoob, Preeraya Singkhaimuk, Chanyapat Nitatsukprasert, Silas A. Davidson and Alongkot Ponlawat

Pathogens 2020, 9(6), 442; https://doi.org/10.3390/pathogens9060442 - 4 Jun 2020

Cited by 12 | Viewed by 3718

Abstract

Entomological surveillance for arthropod-borne viruses is vital for monitoring vector-borne diseases and informing vector control programs. In this study, we conducted entomological surveillance in Zika virus endemic areas. In Thailand, it is standard protocol to perform mosquito control within 24 h of a reported dengue case. Aedes females were collected within 72 h of case reports from villages with recent Zika–human cases in Kamphaeng Phet Province, Thailand in 2017 and 2018. Mosquitoes were bisected into head-thorax and abdomen and then screened for Zika (ZIKV) and dengue (DENV) viruses using real-time RT-PCR. ZIKV RNA was detected in three samples from two female Ae. aegypti (1.4%). A partial envelope sequence analysis revealed that the ZIKV sequences were the Asian lineage identical to sequences from ZIKV-infected cases reported in Thailand during 2016 and 2017. Dengue virus-1 (DENV-1) and dengue virus-4 (DENV-4) were found in four Ae. aegypti females (2.8%), and partial capsid sequences were nearly identical with DENV-1 and DENV-4 from Thai human cases reported in 2017. Findings in the current study demonstrate the importance of entomological surveillance programs to public health mosquito-borne disease prevention measures and control. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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12 pages, 1158 KiB

Open AccessArticle

Highly Efficient Vertical Transmission for Zika Virus in Aedes aegypti after Long Extrinsic Incubation Time

by Menchie Manuel, Dorothée Missé and Julien Pompon

Pathogens 2020, 9(5), 366; https://doi.org/10.3390/pathogens9050366 - 11 May 2020

Cited by 7 | Viewed by 3146

Abstract

While the Zika virus (ZIKV) 2014–2017 pandemic has subsided, there remains active transmission. Apart from horizontal transmission to humans, the main vector Aedes aegypti can transmit the virus vertically from mother to offspring. Large variation in vertical transmission (VT) efficiency between studies indicates the influence of parameters, which remain to be characterized. To determine the roles of extrinsic incubation time and gonotrophic cycle, we deployed an experimental design that quantifies ZIKV in individual progeny and larvae. We observed an early infection of ovaries that exponentially progressed. We quantified VT rate, filial infection rate, and viral load per infected larvae at 10 days post oral infection (d.p.i.) on the second gonotrophic cycle and at 17 d.p.i. on the second and third gonotrophic cycle. As compared to previous reports that studied pooled samples, we detected a relatively high VT efficiency from 1.79% at 10 d.p.i. and second gonotrophic cycle to 66% at 17 d.p.i. and second gonotrophic cycle. At 17 d.p.i., viral load largely varied and averaged around 800 genomic RNA (gRNA) copies. Longer incubation time and fewer gonotrophic cycles promoted VT. These results shed light on the mechanism of VT, how environmental conditions favor VT, and whether VT can maintain ZIKV circulation. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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17 pages, 3831 KiB

Open AccessEditor’s ChoiceArticle

Venereal Transmission of Vesicular Stomatitis Virus by Culicoides sonorensis Midges

by Paula Rozo-Lopez, Berlin Londono-Renteria and Barbara S. Drolet

Pathogens 2020, 9(4), 316; https://doi.org/10.3390/pathogens9040316 - 24 Apr 2020

Cited by 16 | Viewed by 6585

Abstract

Culicoides sonorensis biting midges are well-known agricultural pests and transmission vectors of arboviruses such as vesicular stomatitis virus (VSV). The epidemiology of VSV is complex and encompasses a broad range of vertebrate hosts, multiple routes of transmission, and diverse vector species. In temperate regions, viruses can overwinter in the absence of infected animals through unknown mechanisms, to reoccur the next year. Non-conventional routes for VSV vector transmission may help explain viral maintenance in midge populations during inter-epidemic periods and times of adverse conditions for bite transmission. In this study, we examined whether VSV could be transmitted venereally between male and female midges. Our results showed that VSV-infected females could venereally transmit virus to uninfected naïve males at a rate as high as 76.3% (RT-qPCR), 31.6% (virus isolation) during the third gonotrophic cycle. Additionally, VSV-infected males could venereally transmit virus to uninfected naïve females at a rate as high as 76.6% (RT-qPCR), 49.2% (virus isolation). Immunofluorescent staining of micro-dissected reproductive organs, immunochemical staining of midge histological sections, examination of internal reproductive organ morphology, and observations of mating behaviors were used to determine relevant anatomical sites for virus location and to hypothesize the potential mechanism for VSV transmission in C. sonorensis midges through copulation. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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24 pages, 1229 KiB

Open AccessArticle

A Systematic Review: Is Aedes albopictus an Efficient Bridge Vector for Zoonotic Arboviruses?

by Taissa Pereira-dos-Santos, David Roiz, Ricardo Lourenço-de-Oliveira and Christophe Paupy

Pathogens 2020, 9(4), 266; https://doi.org/10.3390/pathogens9040266 - 7 Apr 2020

Cited by 64 | Viewed by 5337

Abstract

Mosquito-borne arboviruses are increasing due to human disturbances of natural ecosystems and globalization of trade and travel. These anthropic changes may affect mosquito communities by modulating ecological traits that influence the “spill-over” dynamics of zoonotic pathogens, especially at the interface between natural and human environments. Particularly, the global invasion of Aedes albopictus is observed not only across urban and peri-urban settings, but also in newly invaded areas in natural settings. This could foster the interaction of Ae. albopictus with wildlife, including local reservoirs of enzootic arboviruses, with implications for the potential zoonotic transfer of pathogens. To evaluate the potential of Ae. albopictus as a bridge vector of arboviruses between wildlife and humans, we performed a bibliographic search and analysis focusing on three components: (1) The capacity of Ae. albopictus to exploit natural larval breeding sites, (2) the blood-feeding behaviour of Ae. albopictus, and (3) Ae. albopictus’ vector competence for arboviruses. Our analysis confirms the potential of Ae. albopictus as a bridge vector based on its colonization of natural breeding sites in newly invaded areas, its opportunistic feeding behaviour together with the preference for human blood, and the competence to transmit 14 arboviruses. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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Review

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23 pages, 6213 KiB

Open AccessEditor’s ChoiceReview

Mayaro Virus Pathogenesis and Transmission Mechanisms

by Cheikh Tidiane Diagne, Michèle Bengue, Valérie Choumet, Rodolphe Hamel, Julien Pompon and Dorothée Missé

Pathogens 2020, 9(9), 738; https://doi.org/10.3390/pathogens9090738 - 8 Sep 2020

Cited by 47 | Viewed by 7414

Abstract

Mayaro virus (MAYV), isolated for the first time in Trinidad and Tobago, has captured the attention of public health authorities worldwide following recent outbreaks in the Americas. It has a propensity to be exported outside its original geographical range, because of the vast distribution of its vectors. Moreover, most of the world population is immunologically naïve with respect to infection with MAYV which makes this virus a true threat. The recent invasion of several countries by Aedesalbopictus underscores the risk of potential urban transmission of MAYV in both tropical and temperate regions. In humans, the clinical manifestations of MAYV disease range from mild fever, rash, and joint pain to arthralgia. In the absence of a licensed vaccine and clinically proven therapeutics against Mayaro fever, prevention focuses mainly on household mosquito control. However, as demonstrated for other arboviruses, mosquito control is rather inefficient for outbreak management and alternative approaches to contain the spread of MAYV are therefore necessary. Despite its strong epidemic potential, little is currently known about MAYV. This review addresses various aspects of MAYV, including its epidemiology, vector biology, mode of transmission, and clinical complications, as well as the latest developments in MAYV diagnosis. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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14 pages, 1351 KiB

Open AccessEditor’s ChoiceReview

A Review: Wolbachia-Based Population Replacement for Mosquito Control Shares Common Points with Genetically Modified Control Approaches

by Pei-Shi Yen and Anna-Bella Failloux

Pathogens 2020, 9(5), 404; https://doi.org/10.3390/pathogens9050404 - 22 May 2020

Cited by 48 | Viewed by 8869

Abstract

The growing expansion of mosquito vectors has made mosquito-borne arboviral diseases a global threat to public health, and the lack of licensed vaccines and treatments highlight the urgent need for efficient mosquito vector control. Compared to genetically modified control strategies, the intracellular bacterium Wolbachia, endowing a pathogen-blocking phenotype, is considered an environmentally friendly strategy to replace the target population for controlling arboviral diseases. However, the incomplete knowledge regarding the pathogen-blocking mechanism weakens the reliability of a Wolbachia-based population replacement strategy. Wolbachia infections are also vulnerable to environmental factors, temperature, and host diet, affecting their densities in mosquitoes and thus the virus-blocking phenotype. Here, we review the properties of the Wolbachia strategy as an approach to control mosquito populations in comparison with genetically modified control methods. Both strategies tend to limit arbovirus infections but increase the risk of selecting arbovirus escape mutants, rendering these strategies less reliable. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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Other

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11 pages, 937 KiB

Open AccessOpinion

From Anonymous to Public Enemy: How Does a Mosquito Become a Feared Arbovirus Vector?

by Didier Fontenille and Jeffrey R. Powell

Pathogens 2020, 9(4), 265; https://doi.org/10.3390/pathogens9040265 - 5 Apr 2020

Cited by 16 | Viewed by 3450

Abstract

The past few decades have seen the emergence of several worldwide arbovirus epidemics (chikungunya, Zika), the expansion or recrudescence of historical arboviruses (dengue, yellow fever), and the modification of the distribution area of major vector mosquitoes such as Aedes aegypti and Ae. albopictus, raising questions about the risk of appearance of new vectors and new epidemics. In this opinion piece, we review the factors that led to the emergence of yellow fever in the Americas, define the conditions for a mosquito to become a vector, analyse the recent example of the new status of Aedes albopictus from neglected mosquito to major vector, and propose some scenarios for the future. Full article

(This article belongs to the Special Issue Untargeted Alternative Routes of Arbovirus Transmission)

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